Keeping pace with climate change: what is wrong with the evolutionary potential of upper thermal limits?

Abstract

The potential of populations to evolve in response to ongoing climate change is partly conditioned by the presence of heritable genetic variation in relevant physiological traits. Recent research suggests that Drosophila melanogaster exhibits negligible heritability, hence little evolutionary potential in heat tolerance when measured under slow heating rates that presumably mimic conditions in nature. Here, we study the effects of directional selection for increased heat tolerance using Drosophila as a model system. We combine a physiological model to simulate thermal tolerance assays with multilocus models for quantitative traits. Our simulations show that, whereas the evolutionary response of the genetically determined upper thermal limit (CTmax) is independent of methodological context, the response in knockdown temperatures varies with measurement protocol and is substantially (up to 50%) lower than for CTmax. Realized heritabilities of knockdown temperature may grossly underestimate the true heritability of CTmax. For instance, assuming that the true heritability of CTmax in the base population is h2 = 0.25, realized heritabilities of knockdown temperature are around 0.08–0.16 depending on heating rate. These effects are higher in slow heating assays, suggesting that flawed methodology might explain the apparently limited evolutionary potential of cosmopolitan D. melanogaster.

Evolutionary capacity of upper thermal limits: beyond single trait assessments

“…There has subsequently been mounting interest in understanding the extent to which the evolution of upper thermal limits might be constrained by low additive genetic variance (Kellermann et al, 2012;Mitchell and Hoffmann, 2010). It has recently been suggested that inferences about an organisms' ability to evolve higher upper thermal limits will depend on how heat tolerance is measured (Chown et al, 2009;Mitchell and Hoffmann, 2010;Rezende et al, 2011;Santos et al, 2012). Specifically, estimates of heritability using ramping assays may be reduced largely because this measure incorporates more stochasticity, thereby increasing the environmental variance (Chown et al, 2009;Rezende et al, 2011;Santos et al, 2012).…”

“…It has recently been suggested that inferences about an organisms' ability to evolve higher upper thermal limits will depend on how heat tolerance is measured (Chown et al, 2009;Mitchell and Hoffmann, 2010;Rezende et al, 2011;Santos et al, 2012). Specifically, estimates of heritability using ramping assays may be reduced largely because this measure incorporates more stochasticity, thereby increasing the environmental variance (Chown et al, 2009;Rezende et al, 2011;Santos et al, 2012). In the first direct test of these ideas, Mitchell and Hoffmann (Mitchell and Hoffmann, 2010) did indeed show that the narrow-sense heritability for ramping heat knockdown time was not significantly different from zero.…”

“…Narrow-sense heritability estimates for ramping heat knockdown time were not significantly different from zero because of low levels of additive genetic variance for this trait, not because of increased environmental variance (see Santos et al, 2012). Indeed, the environmental variance for ramping heat knockdown time was smaller than for either of the static measures of heat tolerance, as was the mean standardised coefficient of environmental variation.…”

“…Nonetheless, criticism of this and other studies (e.g. Sgrò et al, 2010;van Heerwaarden et al, 2012) that have used slower (0.06°C increase per minute) ramping rates to examine upper thermal limits has continued on the grounds that such rates are Evolutionary capacity of upper thermal limits: beyond single trait assessments Shaun Blackburn, Belinda van Heerwaarden, Vanessa Kellermann and Carla M. Sgrò* confounded by increased stochasticity, which will inflate the environmental variance and subsequently reduce narrow-sense heritability estimates, thereby artificially lowering estimates of adaptive capacity for upper thermal limits Santos et al, 2011;Santos et al, 2012).…”

Eco‐evolution on the edge during climate change

“…Heritabilities are useful under constant conditions, but could misrepresent evolutionary potential in the wild for two reasons (Visscher et al 2008, Hendry 2017. Heritability can therefore be high in nature or the future, even when experiments suggest it is currently low (Santos et al 2012, Heerwaarden et al 2016, Shama 2017. Second, heritabilities differ among populations and environments (Hoffmann and Merilä 1999), yet most heritability estimates derive from a few populations and under restrictive environmental (often laboratory) conditions.…”